The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach

Journal of Anatomy

Volumn 220, Issue 6, 2012, Pages 529-543

  Gunz, Philipp ^a   Ramsier, Marissa ^a,b   Kuhrig, Melanie ^a   Hublin, Jean Jacques ^a   Spoor, Fred ^a,c  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b HUMBOLDT STATE UNIVERSITY   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cochlea; Inner ear; Primate; Procrustes; Semicircular canals; Semilandmarks; Shape space

Indexed keywords

ARTICLE; COCHLEA; COMPUTER ASSISTED TOMOGRAPHY; GEOMETRY; HUMAN; INNER EAR; MAMMAL; MORPHOMETRICS; NONHUMAN; PAN TROGLODYTES; PHYLOGENY; PRIMATE; PRIORITY JOURNAL; SEMICIRCULAR CANAL; TEMPORAL BONE; THREE DIMENSIONAL IMAGING;

ANIMALS; EAR, INNER; FEMALE; HUMANS; MALE; MEDICAL ILLUSTRATION; PAN TROGLODYTES; TEMPORAL BONE; TOMOGRAPHY, X-RAY COMPUTED;

MAMMALIA; PAN; PAN TROGLODYTES TROGLODYTES; PRIMATES; THERIA;

EID: 84860449552     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2012.01493.x     Document Type: Article

References (71)

1. Blanks RH, Curthoys IS, Bennett ML, et al. (1985) Planar relationships of the semicircular canals in rhesus and squirrel monkeys. Brain Res 340, 315-324.
2. Boesch C, Boesch-Achermann H (2000) The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution. Oxford: Oxford University Press.
3. Boesch C, Kohou G, Néné H, et al. (2006) Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130, 103-115.
4. Bookstein FL (1989) Principal warps: thin-plate splines and the decomposition of deformations. IEEE Trans Pattern Anal Mach Intell V, 567-585.
5. Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press.
6. Bookstein FL (1997) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med Image Anal 1, 225-243.
7. Bradshaw AP, Curthoys IS, Todd MJ, et al. (2010) A mathematical model of human semicircular canal geometry: a new basis for interpreting vestibular physiology. J Assoc Res Otolaryngol 11, 145-159.
8. Christensen GE, He J, Dill JA, et al. (2003) Automatic measurement of the labyrinth using image registration and a deformable inner ear atlas. Acad Radiol 10, 988-999.
9. Coleman MN, Colbert MW (2010) Correlations between auditory structures and hearing sensitivity in non-human primates. J Morphol 271, 511-532.
10. Cox PG, Jeffery N (2008) Geometry of the semicircular canals and extraocular muscles in rodents, lagomorphs, felids and modern humans. J Anat 213, 583-596.
11. Cox PG, Jeffery N (2010) Semicircular canals and agility: the influence of size and shape measures. J Anat 216, 37-47.
12. Curthoys IS, Oman CM (1987) Dimensions of the horizontal semicircular duct, ampulla and utricle in the human. Acta Otolaryngol 103, 254-261.
13. Curthoys IS, Blanks RH, Markham CH (1977) Semicircular canal radii of curvature (R) in cat, guinea pig and man. J Morphol 151, 1-15.
14. David R (2011) Le système des canaux semi-circulaires des archosaures: anatomie, morphométrie, morphologie fonctionnelle, évolution. PhD thesis, Paris: Museum National d'Histoire National.
15. David R, Droulez J, Allain R, et al. (2010) Motion from the past. A new method to infer vestibular capacities of extinct species. CR Palevol, 9, 397-410.
16. Ekdale EG, Rowe T (2011) Morphology and variation within the bony labyrinth of zhelestids (Mammalia, Eutheria) and other therian mammals. J Vertebr Paleontol 31, 658-675.
17. Fleischer G (1973) Studien am Skelett des Gehörorgans der Säugetiere, einschließlich des Menschen. Säugetierkundliche Mitteilungen 21, 131-239.
18. Fleischer G (1976) Hearing in extinct cetaceans as determined by cochlear structure. J Paleontol 50, 133-152.
19. Georgi JA, Sipla JS (2008) Balance: comparative and functional anatomy in aquatic reptiles and birds. In Sensory Evolution on the Threshold, Adaptations in Secondarily Aquatic Vertebrates (eds Thewissen JGM, Nummela S), pp. 233-256. Berkley: University of California Press.
20. Good PI (2000) Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses. New York: Springer.
21. Gray AA (1907) The Labyrinth of Animals, Vol. 2. London: Churchill.
22. Gray AA (1908) The Labyrinth of Animals: Including Mammals, Birds, Reptiles and Amphibians. London: Churchill.
23. Gunz P (2005) Statistical and Geometric Reconstruction of Hominid Crania: Reconstructing Australopithecine Ontogeny. PhD dissertation, Vienna: University of Vienna.
24. Gunz P, Harvati K (2007) The Neanderthal 'chignon': variation, integration, and homology. J Hum Evol 52, 262-274.
25. Gunz P, Mitteroecker P, Bookstein FL (2005) Semilandmarks in three dimensions. In Modern Morphometrics in Physical Anthropology (ed. Slice DE), pp. 73-98. New York: Kluwer Academic/Plenum Publishers.
26. Gunz P, Mitteroecker P, Neubauer S, et al. (2009a) Principles for the virtual reconstruction of hominin crania. J Hum Evol 57, 48-62.
27. Gunz P, Spoor F, Tilgner R, et al. (2009b) The Neanderthal bony labyrinth reconsidered, introducing a new geometric morphometric approach. Am J Phys Anthropol 138(S48), 142.
28. Hublin JJ, Spoor F, Braun M, et al. (1996) A late Neanderthal associated with Upper Palaeolithic artefacts. Nature 381, 224-226.
29. Hullar TE (2006) Semicircular canal geometry, afferent sensitivity, and animal behavior. Anat Rec A Discov Mol Cell Evol Biol 288, 466-472.
30. Hyrtl J (1845) Vergleichend-anatomische Untersuchungen über das innere Gehörorgan des Menschen und der Säugethiere: Mit neun Kupfertafeln. Prague: Verlag von Friedrich Ehrlich.
31. Ifediba MA, Rajguru SM, Hullar TE, et al. (2007) The role of 3-canal biomechanics in angular motion transduction by the human vestibular labyrinth. Ann Biomed Eng 35, 1247-1263.
32. Jeffery N, Cox PG (2010) Do agility and skull architecture influence the geometry of the mammalian vestibulo-ocular reflex? J Anat 216, 496-509.
33. Jeffery N, Spoor F (2004) Prenatal growth and development of the modern human labyrinth. J Anat 204, 71-92.
34. Jeffery N, Spoor F (2006) The primate subarcuate fossa and its relationship to the semicircular canals part I: prenatal growth. J Hum Evol 51, 537-549.
35. Ketten DR, Wartzok D (1990) Three-dimensional reconstructions of the dolphin ear. In Sensory Abilities of Cetaceans: Laboratory and Field Evidence (eds Thomas J, Kastelein R), pp. 81-105. New York: Plenum Press.
36. Kirk EC, Gosselin-Ildari AD (2009) Cochlear labyrinth volume and hearing abilities in primates. Anat Rec 292, 765-776.
37. Ladevèze S, de Muizon C, Colbert M, et al. (2010) 3D computational imaging of the petrosal of a new multituberculate mammal from the Late Cretaceous of China and its paleobiologic inferences. CR Palevol 9, 319-330.
38. Lebrun R, De León MP, Tafforeau P, et al. (2010) Deep evolutionary roots of strepsirrhine primate labyrinthine morphology. J Anat 216, 368-380.
39. Luo Z, Ketten DR (1991) CT scanning and computerized reconstructions of the inner ear of multituberculate mammals. J Vertebr Paleontol, 11, 220-228.
40. Luo ZX, Ruf I, Schultz JA, et al. (2011) Fossil evidence on evolution of inner ear cochlea in Jurassic mammals. Proc R Soc B 278, 28-34.
41. Macrini TE, Flynn JJ, Croft DA, et al. (2010) Inner ear of a notoungulate placental mammal: anatomical description and examination of potentially phylogenetically informative characters. J Anat 216, 600-610.
42. Malinzak MD (2010) Experimental Analyses of the Relationship between Semicircular Canal Morphology and Locomotor Head Rotations in Primates. PhD dissertation, Department of Biological Anthropology and Anatomy, Duke University.
43. Matano S, Kubo T, Niemitz C, et al. (1985) Semicircular canal organ in three primate species and behavioral correlations. Fortschr Zool 30, 677-680.
44. Mitteroecker P, Bookstein F (2011) Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 38, 100-114.
45. Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36, 235-247.
46. Ni X, Flynn JJ, Wyss AR (2010) The bony labyrinth of the early platyrrhine primate Chilecebus. J Hum Evol 59, 595-607.
47. Ramprashad F, Landolt JP, Money KE, et al. (1984) Dimensional analysis and dynamic response characterization of mammalian peripheral vestibular structures. Am J Anat 169, 295-313.
48. Rogers SW (1999) Allosaurus, crocodiles, and birds: evolutionary clues from spiral computed tomography of an endocast. Anat Rec 257, 162-173.
49. Rohlf FJ, Marcus LF (1993) A revolution in morphometries. Trends Ecol Evol 8, 129-132.
50. Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39, 40-59.
51. Rook L, Bondioli L, Casali F, et al. (2004) The bony labyrinth of Oreopithecus bambolii. J Hum Evol 46, 349-356.
52. Schmelzle T, Sánchez-Villagra MR, Maier W (2007) Vestibular labyrinth diversity in diprotodontian marsupial mammals. Mammal Study 32, 83-97.
53. Silcox MT, Bloch JI, Boyer DM, et al. (2009) Semicircular canal system in early primates. J Hum Evol 56, 315-327.
54. Sipla JS (2007) The Semicircular Canals of Birds and Non-Avian Theropod Dinosaurs. PhD dissertation, Department of Anatomical Sciences, Stony Brook University.
55. Skinner MM, Gunz P, Wood BA, et al. (2008) Enamel-dentine junction (EDJ) morphology distinguishes the lower molars of Australopithecus africanus and Paranthropus robustus. J Hum Evol 55, 979-988.
56. Skinner MM, Gunz P, Wood BA, et al. (2009) Discrimination of extant Pan species and subspecies using the enamel-dentine junction morphology of lower molars. Am J Phys Anthropol 140, 234-243.
57. Slice DE (2007) Geometric morphometrics. Annu Rev Anthropol 36, 261-281.
58. Spoor CF (1993) The Comparative Morphology and Phylogeny of the Human Bony Labyrinth. PhD dissertation, Utrecht: Universiteit Utrecht.
59. Spoor F, Thewissen JGM (2008) Balance: comparative and functional anatomy in aquatic mammals. In Sensory Evolution on the Threshold, Adaptations in Secondarily Aquatic Vertebrates (eds Thewissen JGM, Nummela S), pp. 257-284. Berkeley: University of California Press.
60. Spoor F, Zonneveld F (1995) Morphometry of the primate bony labyrinth: a new method based on high-resolution computed tomography. J Anat 186(Pt 2), 271-286.
61. Spoor F, Zonneveld F (1998) Comparative review of the human bony labyrinth. Yearbook Phys Anthropol 41, 211-251.
62. Spoor CF, Zonneveld FW, Macho GA (1993) Linear measurements of cortical bone and dental enamel by computed tomography: applications and problems. Am J Phys Anthropol 91, 469-484.
63. Spoor F, Wood B, Zonneveld F (1994) Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369, 645-648.
64. Spoor F, Bajpai S, Hussain ST, et al. (2002a) Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417, 163-166.
65. Spoor F, Esteves F, Tecelão Silva F, et al. (2002b) The bony labyrinth of Lagar Velho 1. In The Lapedo Child, A Gravettian Human Skeleton from the Abrigo do Lagar Velho (eds Zilhão J, Trinkaus E, Duarte C), pp. 287-292. Lisbon: Trabalhos de Arqueologia, 22, Instituto Portugues de Arqueologia.
66. Spoor F, Hublin JJ, Braun M, et al. (2003) The bony labyrinth of Neanderthals. J Hum Evol 44, 141-165.
67. Spoor F, Garland T, Krovitz G, et al. (2007) The primate semicircular canal system and locomotion. Proc Natl Acad Sci U S A 104, 10808-10812.
68. Takahashi H (1971) [Comparative anatomical studies of bony labyrinths of the inner ears in Canidae]. Kaibogaku Zasshi 46, 85-98.
69. Takahashi H (1976) [Comparative anatomical study of the bony labyrinth of the inner ear of primates]. Kaibogaku Zasshi 51, 366-387.
70. Walker A, Ryan TM, Silcox MT, et al. (2008) The semicircular canal system and locomotion: the case of extinct lemuroids and lorisoids. Evol Anthropol 17, 135-145.
71. Yamada M, Yoshizaki F (1959) Osseous labyrinth of Cetacea. Sci Rep Whales Res Inst, Tokyo 14, 291-304.